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Cien. Inv. Agr. 34(3): 125-142.

2007
www.rcia.puc.cl

LITERATURE REVIEW

Leafminer parasitoids and pest management

Adriana Salvo1 and Graciela R. Valladares


Centro de Investigaciones Entomolgicas de Crdoba, Instituto Multidisciplinario de Biologa Vegetal.
Consejo Nacional de Investigaciones Cientficas y Tecnolgicas.
Facultad de Ciencias Exactas, Fsicas y Naturales. Universidad Nacional de Crdoba.
Av. Vlez Sarsfield 1611. X5016GCA. Crdoba, Argentina.

Abstract

A. Salvo, and G.R. Valladares. 2007. Leafminer parasitoids and pest management. Cien.
Inv. Agr. 34(3):125-142. Leafminers are insects whose larvae live and feed within plant
leaves, consuming mesophyll tissue without damaging the leaf epidermis. Several species are
considered serious pests on intensive, horticultural, and ornamental crops. Natural enemies
are the most frequent source of mortality for this herbivore insect guild, with parasitoids being
the most effective and best represented source. This article provides an updated summary of
the available research on leafminer parasitoids in relation to pest management. Parasitoids of
leafminers are predominantly generalists, and can thus rapidly include in their host ranges newly
introduced leafminer species, frequently achieving effective regulation a few years after the
pest becomes established. Classical and augmentative biological control strategies are broadly
used for leafminer pest management. Several studies have dealt with the simultaneous use of
parasitoids together with chemical and cultural control. Many conventional insecticides have
detrimental effects on parasitoids; however, others could be compatible with biological control.
Although integrated pest management programs employing a combination of several control
strategies have achieved success against leafminer pests, the effects of cultural practices that
could boost parasitoid populations have been scarcely studied.

Key words: Biological control, chemical control, cultural control, leafminers, parasitoids, pest
management.

Introduction to their hosts particular conditions of life, and


have great potential in biological pest control
Parasitoids are insects with a complex and programs (Hawkins et al., 1993).
fascinating biology, whose larvae feed on
other insects, killing them in order to complete This article includes a review of leafminer parasit-
their development. Although they are usually oids in the context of their potential use in insect
unnoticed due to their small size, this group pest management. For this, we reviewed the eco-
of organisms has tremendous economic logical literature referring to both theoretical and
importance, as they regulate the population of practical aspects that must be considered when
their hosts and thereby represent useful tools for using leafminer parasitoids as population regula-
insect pest management. Leafminer parasitoids tors. Likewise, other strategies used in the control
constitute an interesting and relatively well- of leafminers are discussed, with an emphasis on
studied group of species belonging to at the relationship between these methods and the
least ten families of the Order Hymenoptera, regulation exercised by the parasitoids. The sub-
Suborder Apocrita. These insects have adapted ject is introduced with a brief characterization of
leafminer insects, their economic importance, the
reasons why several species reach pest status in
Received 07 June 2007. Accepted 23 July 2007.
various crops, and the relative importance of par-
1
Corresponding author: asalvo@efn.uncor.edu asitoids for the regulation of their populations.
126 CIENCIA E INVESTIGACION AGRARIA

The leafminers the same time, leafminer adults have developed


resistance, going from being secondary pests to
Leafminers are insects whose larvae live and becoming primary pests (Murphy and La Salle,
feed inside the leaves, consuming the mesophyll 1999; Civelek and Weintraub, 2003). Concrete
without damaging the leaf epidermis. Their examples of this are Liriomyza sativae (Hills
feeding tracks (mines) are externally visible and Taylor, 1951), L. trifolii (Reitz et al., 1999),
in leaves, as whitish or grey areas with variable leafminers of the genus Phyllonorycterr on fruit
shapes that rangefrom narrow linear galleries trees (Maier, 2001), and several leafminer pests
to wide chambers (Hering, 1951). The leaf on tomatoes (Gelenter and Trumble, 1999).
mining habit has been developed by a group
of over 10,000 species of holometabolous Another factor that could contribute to certain
insects, concentrated in four orders: Diptera, leafminer species becoming pests is the
Coleoptera, Hymenoptera, and Lepidoptera increase in monocultivation. Many parasitoids
(Connor and Taverner, 1997). have preference for specific plants. Therefore,
if the only crop present is not attractive
The galleries excavated by the leafminer larva for the parasitoids, leafminers may escape
can reduce the photosynthetic capacity of leaves, parasitoidism in this environment (Murphy and
cause premature leaf abscission, and permit La Salle, 1999). Finally, the increase of extensive
pathogen entry into plant tissue. Moreover, they horticulture and plant commercialization
reduce the esthetic value of ornamental plants without appropriate quarantine controls has
or edible leaves (Spencer, 1973; Parrella and also favored the expansion of leafminer pest
Jones, 1987; Minkenberg and Van Lenteren, distribution.
1986; Maier, 2001; Valladares, in press). Many
species are considered pests in several parts of Causes of leafminer mortality
the world. Among these are the citrus leafminer
Phyllocnistis citrella Stainton (Lepidoptera: Intraspecific competition, both direct by
Gracillariidae), and more than 100 species interference, or indirect or exploitive, represents
of leaf mining flies (Diptera: Agromyzidae), an important cause of mortality for the leafminer
especially Liriomyza trifolii (Burgess) and larvae (Faeth, 1990; Auerbach et al., 1995; Eber,
Liriomyza huidobrensis (Blanchard) in 2004). Leaf abscission has also been indicated
horticultural crops, and Agromyza frontella as another important survival factor for
(Rondan) in alfalfa (Amalin, et al. 2002; leafminers (Potter, 1985; Faeth, 1990; Girardoz
Dempewolf, 2004). et al., 2006a). Abscission can be interpreted as
the plant defense induced by leafminer attack.
Most authors agree that a leafminer species Nevertheless, in some cases, it could benefit
becomes a pest due to insecticide resistance the leafminers by freeing them from potential
development and the elimination of their parasitoid attack (Kahn and Cornell, 1989). On
natural enemies. The latter is a consequence of the other hand, some leaf mining larvae release
aggressive agricultural practices (i.e. plowing, cytokinins that maintain green areas (green
breaking up, and burning of soils, etc.) and the use islands) in ageing leaves, which allows them
of agrochemicals (Spencer, 1973; Minkenberg to complete their development. Stiling and
and Van Lenteren, 1986). Furthermore, another Simberloff (1989), after studying the mortality
two factors can importantly contribute to of some species that induce leaf abscission,
elevate leafminer population sizes: 1. Relative conclude that this phenomenon must be seen,
inconspicuousness, allowing them to go from a parsimonious point of view, as a simple
unnoticed until reaching high densities (Maier, response of the plant to the phytophagous
2001), and 2. The protection of their immature damage. Other plant defense mechanisms,
stages inside plant tissue, especially against mostly related to chemical and physical aspects,
the effects of contact insecticides. This last have also been mentioned (Valladares and
characteristic has promoted the indiscreet use Lawton, 1991).
of wide spectrum insecticides, which have
decimated their natural enemy populations. At The action of natural enemies occurs by
VOL 34 N3 SEPTEMBER - DECEMBER 2007 127

predation and parasitoidism. Predation has been parasitoids (Hochberg and Hawkins, 1992).
cited as the greatest cause of mortality at the On the other hand, leafminers are herbivorous
beginning of the growing season of some crops, insects characterized by a distinct homogeneity
while parasitoidism is more important in more of both ecological and taxonomic aspects
advanced stages of crop development (Queiroz, (Connor and Taverner 1997), which facilitates
2002; Urbaneja et al., 2000). Except for some the development of a diverse community of
leafminers, such as Tuta absoluta (Lepidoptera: parasitoids that share hosts, and would explain
Gelechiidae), very low mortality values due to why this insect group as a whole has an elevated
parasitoidism (<1%) and high levels of larval load of parasitic species (Godfray, 1994).
mortality due to predation, which can reach up
to 80% (Motta Miranda et al., 1998), have been Most of the leafminer parasitoid species
reported. correspond taxonomically to the superfamilies
Chalcidoidea (Families Eulophidae and
Leafminer predators include birds, spiders and Pteromalidae), Ichneumonoidea (Family
insects. Among the insects, there are predators Braconidae), and Cynipoidea (Family Figitidae)
in various families of Coleoptera (ej. Carabidae, (Salvo, in press). These insects may be classified
Cicindelidae, Staphylinidae), Hemiptera (i.e. as idiobionts, when they permanently paralyze
Anthocoridae, Nabidae, Lygaeidae), and their host when ovipositing, or as koinobionts,
Hymenoptera (i.e. ants) (Cisneros and Mujica, which only temporarily paralyzes the host,
1998; Motta Miranda et al., 1998; Arno et al., allowing it to continue its development prior to
2003; Grabenweger et al., 2005). The effect provoking its death (Askew and Shaw, 1986).
of predators sometimes surpasses the effect of The idiobiont/koinobiont dichotomy would
parasitoidism (Memmott et al., 1993; Queiroz, be associated with a series of differentiating
2002; Xiao et al., 2007); furthermore, they can characteristics related to their host groups
even have an adverse effect on the mortality preference, feeding specificity, reproductive
caused by parasitoids (Sato and Higashi, strategy, development time, competitive
1987). capacity, presence of sexual dimorphism, etc.
(Gauld and Bolton, 1988; Salvo and Valladares,
Although the relative influence of predators and 1999).
parasitoids in regulating different leafminer
species is variable, the literature indicates The idiobionts, by permanently paralyzing their
that, in general, the parasitoids constitute hosts, risk the possibility that their food resource
the most important group (Parrella, 1987; will later be attacked by other organisms,
Hespenheide, 1991). Parasitoids have a key so they are more frequently associated with
function in leafminer population control in endophytophagous insects, which feed inside
natural ecosystems and in cultivated areas plant tissues and are better protected from
with a rational use of insecticides (Lewis et al., unfavorable conditions (Quicke, 1997). On the
2002). other hand, by attacking a resource without
physiological defenses, the idiobionts could
The leafminer parasitoids consume a greater variety of hosts.

The leafminers are in the phytophagous guild Conversely, the koinobionts must coexist
(group of organisms that consume the same for some time with an active organism and,
resource in the similar manner), which has the therefore, are restricted to fewer host species.
greatest number of parasitoid species per host Since leafminers are endophagous insects, it
species, and has the highest average rate of is expected that their parasitic complexes will
parasitoidism (Hawkins, 1994). Characteristics be dominated by idiobiont species (Hawkins,
of leafminer habits, such as the scarce mobility 1994), which is not always the case (Salvo,
of the larvae, the clear visibility of the mines 1996).
produced, and the scarce physical protection
provided by the leaf epidermis, are the In terms of food specificity, the literature
main causes of leafminers vulnerability to contributes abundant evidence that leafminer
128 CIENCIA E INVESTIGACION AGRARIA

parasitoids have ample food ranges, generally expected mortality levels (Grabenweger, 2004),
defined by the host ecology (Godfray, 1994; which may be due to poor synchronization
Salvo and Valladares, 1999). This wide food between pests and parasitoids, or to the lack
range has interesting consequences regarding of density-dependent responses (degree of
introduced species management, since it allows response dependent on population density)
the leafminer parasitoids present in an area (Malausa, 1997; Girardoz et al., 2006b).
to incorporate the invasive species into their
spectrum of hosts in relatively short periods of The efficiency of parasitoids as agents of
time (Murphy and La Salle, 1999). In effect, leafminer mortality varies depending on
when a leafminer species invades a new region the species, and it may even vary between
and becomes a pest, it initially possesses a low different larval stages of the same species, as
number of associated parasitic species, and they well as in relation to environmental conditions
are mostly generalist idiobionts with low rates of (Grabenweger, 2003). For example, parasitoids
parasitoidism. However, the new leafminers are are likely to be a more important cause of
soon colonized by other parasitoids and reach mortality in temperate zones than in the tropics
total parasitoidism levels similar to that of native (Hawkins et al., 1997; Queiroz, 2002). Similarly,
leafminers, which is often sufficient to achieve parasitoidism rates would be higher at the end
natural control. For example, this process has of the growing season, at least in cultivated
been observed in Phyllocnistis citrella Stainton systems (Parrella, 1987; Murphy and La Salle,
(Lepidoptera: Gracillariidae) in diverse regions 1999; Urbaneja et al., 2000). The presence of
of the world (Uygun et al., 1997; Urbaneja et al., other organisms may also affect leafminer
2000; Amalin et al., 2002; Vercher et al., 2005; parasitoidism rates; in this regard, there is
Diez et al., 2006). However, on occasion, the evidence of effects caused by other herbivorous
recruiting of a parasitic complex similar to that insects, such as externally chewing herbivores
of other leafminers is not accompanied by the (Faeth, 1985), and even by the presence of
endophytic fungi (Preszler et al., 1996).

Tritrophic plant-herbivore-parasitoid interac-


tions are important in these systems (Price et al.,
1980). It has been observed that parasitoidism
may also vary depending on plant species
(Olivera and Bordat 1996; Rauf and Shepard,
1999), or even between cultivars or genotypes
of the same plant species in which the leafminer
develops (Fritz et al., 1997; Braman et al., 2005).
For example, L. huidobrensis parasitoidism in
potato is very low compared to that observed in
other crops (Shepard et al., 1998). According to
Johnson and Hara (1987), effective biological
B control of certain leafminers may depend
on the plant species on which the leafminer
feeds. One aspect related to the leafminer
host plant that may affect their parasitoidism
level, mentioned earlier, is leaf abscission. In
some cases, leaf abscission causes mortality
to both the leafminer and parasitoid (Potter,
1985), while in other systems, the abscission
reduces larvae parasitoidism due to the fact
that parasitoids dont search for hosts in fallen
Figure 1. Leafmine of Liriomyza commelinae (Frost) leaves (Kahn and Cornell, 1989).
(Diptera: Agromyzidae). A. Leafmine on Commelina erecta
L. (Commelinaceae). B. Female parasitoid, Chrysocharis
fl acilla (Hymenoptera: Eulophidae) searching for its host. Finally, other factors that affect leafminer
VOL 34 N3 SEPTEMBER - DECEMBER 2007 129

parasitoidism include: droughts (Staley et al., can also affect other aspects in the parasitoid-
2006), leaf age (Facknath, 2005), and leafminer leafminer relationship, like searching behavior
position in the plant (Barrett, 1994; van der (Connor and Cargain, 1994).
Linden 1994; Brown et al., 1997).
Biological control
In parasitoid insects, as well as parasitoidism
itself, there are two other behaviors that may Cases of leafminer biological control, cited in
increase leafminer mortality: 1. feeding on the the literature, mainly report on the introduction
host (host feeding) and 2. host paralyzation and augmentative release of parasitoid insects,
without oviposition or feeding (host stinging). although other organisms have also been
employed, such as nematodes and bacteria
In the first case, adult wasps feed on a certain (Sher et al., 2000; van Mele and van Lenteren
proportion of leafminer larvae, which may or 2002; Cikman and Comelkcloglu, 2006). There
may not be a previous requisite for egg laying are numerous successful examples of classic
(Jervis and Kidd, 1986). Some parasitoids use biological control (introduction of agents for
hosts of different sizes, either as a substrate for the control of a native or foreign pest) with
egg laying or to feed upon (Duncan and Pea, parasitoids for different species of leafminers,
2000). The magnitude of the mortality due to both in the open field (Dharmadhikari et al.,
host feeding may be similar to, or even higher 1977; Johnson et al., 2003; Garca-Mar et al.,
than, that caused by the parasitoidism itself 2004) and in greenhouses (van Lenteren and
(Amalin et al., 2002; Bernardo et al., 2006). Woets, 1988; Heinz and Parrella, 1990; Abd-
However, the effect of host feeding, functionally Rabou, 2006). In these cases, studies prior
comparable to predation, is frequently ignored. to introduction are important and include
This may greatly underestimate the levels of tolerance to humidity, ability to recognize
mortality caused by parasitoid species (Cure previously parasitized hosts, existence of
and Cantor, 2003). alternative hosts, as well as synchronization
with the host (Wang et al., 1999; Grabenweger,
In some leafminer parasitoid species, particu- 2004; Girardoz et al., 2006b; Zappala and
larly belonging to the genera Diglyphus Walker, Hoy, 2004). Temperature constraints have also
Sympiesis Foerster and Pnigalio Schrank been shown to be an obstacle for a leafminer
(Hymenoptera, Eulophidae), paralyzation and parasitoid to be successfully introduced in
death of leafminer larvae are often observed some regions (Klapwijk et al., 2005; Llcer et
without them being used as an ovipositon al., 2006).
substrate or to feed on (Casas, 1989). This
behavior, interpreted as a way to decrease Large-scale rearing of parasitoids for leafminer
the number of leafminer larvae in the plant control has been considered in the literature
to ensure the survival of the parasitized ones, (Parrella et al., 1989; Kharrat and Jerraya,
varies with the size of the hosts availability, 2005). Diverse factors have been mentioned
their density, the size of cages in which the as important at the time of carrying out large-
parasitoids are reared, and temperature (Heinz scale rearing, among which can be highlight
and Parrella, 1989; Patel and Schuster, 1991; humidity, photoperiod, and temperature (Yoder
Patel et al., 2003). and Hoy 1998; Urbaneja et al., 2001; Lim et al.,
2006; Kafle et al., 2005; Haghani et al., 2007).
Density-dependence in parasitoidism is a
phenomena usually considered favorable for Large-scale rearing of parasitoids implies
host population regulation to be effective simultaneous management of three trophic
(Connor and Beck, 1993; Eber et al., 2001). In levels, which can be difficult (Smith and Hoy,
some cases, the parasitoidism caused by native 1995). The costs and benefits for rearing
parasitoids is more coupled to the density of an parasitoids should be carefully analyzed, and
exotic leafminer than the parasitoidism caused various modifications have been proposed
by the parasitoids introduced for their control in order to get positive results based on
(Amalin et al., 2002). The density of hosts conventional techniques (Rizqi et al., 1999). The
130 CIENCIA E INVESTIGACION AGRARIA

overproduction of males in large-scale parasitoid species would be more effective in regulating


rearing increases the costs of biological control the pest than various species. Some studies
because only females kill the hosts. For this, using leafminer parasitoids indicate that two
techniques have been developed to significantly species released together do not control the host
increase the proportion of females by means of better than when releasing only one (Bader et
using different sized hosts (Ode and Heinz, al., 2006). To establish a priori the feasibility
2002; Chow and Heinz, 2006). of multiple introductions, various laboratory
studies have been carried out to determine
The size of the leafminers may not only affect the role of competition and interference in
the sex ratio but also the size of the parasitoids leafminer parasitoids (Heimpel and Meloche,
reared on them, which could have consequences 2001; Urbaneja et al., 2003; Mitsunaga and
on their reproductive capacity (Abe et al., 2005). Yano, 2004), and also the possible interaction
Intraspecific differences in body size have been between predators and parasitoids (Wu and
observed, for both parasitoids that develop in Lin, 1998).
different host species (Salvo and Valladares,
1996), as well as for those that parasitoidize The simultaneous introduction of parasitoids
the same polyphagous leafminer species and nematodes has been analyzed, with
that reach different body sizes on different conflicting results: in some cases, parasitized
host plants (Salvo and Valladares, 2002). leafminer larvae were infected by the nematode,
Studies on Diglyphus websteri (Crawford) which reduced the survival of the leafminer and
(Hymenoptera: Eulophidae) laboratory rearing the parasitoid as well (Head et al., 2003), while
demonstrated the effects of temperature, host in other cases, there was compatibility between
species, and sex ratio on the size and other the parasitoids and nematodes (Shanower et
growth parameters of the species reared. al., 1992). A crucial element could be the time
Complicated interactions between sex ratio- at which each enemy is released in the field.
temperature, host-temperature, and host- sex There are examples in which the application
ratio-temperature (Bazzocchi et al., 2003) have of nematodes after the release of parasitoids
been also observed. . increased the degree of control, but when
applied before the impact was negative (Sher et
A decrease in the proportion of males can be al., 2000). In the context of simultaneous use
induced through the use of bacteria (Argov et of parasitoids and other organisms, the use of
al., 2000). Species of Wolbachia are one of Bacillus thuringiensis is worth mention, and
the most ubiquitous bacteria in insects, which has shown good results against some leafminer
manipulates the reproduction of the host in species (Khyami-Horani and Ateyyat, 2002),
several ways, among which can be mentioned including some positive effects on the parasitoids
cytoplasmic incompatibility, male death, (Cikman and Comelkcloglu, 2006).
feminization of genetic males, and induction of
parthenogenesis (West et al., 1998). It has been Parasitoids and chemical control
proposed that infected wasps could be more
efficient as leafminer biological control agents In regard to chemical control, most leafminers
(Tagami et al., 2006a,b). are resistant to organophosphorates, carbamates,
and pyrethroids, and at the same time, their
It is important to keep in mind that adults natural enemies are severely damaged by
obtained in the laboratory may exhibit these chemicals, which leave few options for
differences in parasitoidism and host-feeding their chemical control. Insecticides that do
capacity in relation to adults obtained in the not penetrate the leaf surface are practically
field (Arno et al., 2003). Therefore, quality ineffective (Weintraub and Horowitz, 1999). For
control studies of parasitoids obtained through this reason, insecticides with good translaminar
large-scale rearing methods are required. action (i.e. cyromazine and abamectin) are the
most widely used against leafminers (Civelek
A long debate, at the time of introducing natural and Weintraub, 2003). Growth inhibitors are
enemies, consists in knowing if one single useful in controlling leafminers, and at the same
VOL 34 N3 SEPTEMBER - DECEMBER 2007 131

Table 1. Studies evaluating the toxicity of several chemical substances for parasitoids of leafminers.

Pesticides Toxicity1
High Moderated Low

Acetamiprid Mafi and Ohbayashi, 2006 Hidrayani et al., 2005


Alanycarb Mafi and Ohbayashi, 2006 Weintraub and Horowitz, 1998 Parrella and Kaspi, 2005
Abamectin Schuster, 1994 Prijono et al., 2004
Villanueva-Jimnez and Hoy, 1998
Weintraub, 1999; Shen et al., 2003
Bjorksten and Robinson, 2005
Parrella and Kaspi, 2005.
Bifenthrin Mafi and Ohbayashi, 2006
Carbosulfan Hidrayani et al., 2005
Cloropyrifos Prijono et al.,2004
Clothianidin Mafi and Ohbayashi, 2006 Mafi and Ohbayashi, 2006
Cyromazin Weintraub and Horowitz, 1998 Weintraub, 1999; Shen et al.,
Weintraub, 1999. 2003; Prijono et al., 2004;
Bjorksten and Robinson, 2005
Diflubenzuron van Driesche et al., 1998 Villanueva-Jimnez and Hoy,
1998; Mafi and Ohbayashi,
2006
Dimetoato Darvas and Andersen, 1999
Dinotefuran Mafi and Ohbayashi, 2006
Etofenprox Saito 2004
Fenoxycarb Parrella et al., 1983;
Grenier and Grenier, 1993;
Villanueva-Jimnez and
Hoy, 1998.
Fenvalerato Rathman et al., 1990
Flufenoxuron Shen et al., 2003
Imidacloprid Villanueva-Jimnez and Hoy, 1998; Mafi and Ohbayashi, 2006 Villanueva-Jimnez and
Tran et al., 2005 Hoy, 1998.
Isoxathion Mafi and Ohbayashi, 2006
Lufenuron Tran et al., 2005
Mancozeb van Driesche et al., 1998 Prijono et al., 2004;
Bjorksten and Robinson, 2005
Methomyl Saito, 2004 van Driesche et al., 1998 Rathman et al., 1990
Milbemectin Ohno et al., 1999
Mineral oil Conti et al., 2004, Villanueva-Jimnez and
Mafi and Ohbayashi, 2006 Hoy, 1998
Neem and other Conti et al., 2004 Villanueva-Jimnez and
natural products Hoy, 1998; Immaraju, 1998;
Abou-Fakhr Hammad et al.,
2000; Banchio et al., 2003;
Chen et al., 2003a;
Shen et al., 2003.
Organophosphates Villanueva-Jimnez and Hoy, 1998 Rathman et al., 1990
Othion Villanueva-Jimnez and Hoy, 1998
Oxamyl van Driesche et al.,1998 Rathman et al., 1990
Permethrin Saito 2004 Rathman et al., 1990
Pimetrozin Tran et al., 2005
Profenofos Hidrayani et al., 2005
Prothiofos Saito, 2004
Teflubenzuron Mafi and Ohbayashi, 2006
Thiamethoxam Mafi and Ohbayashi, 2006

1
Given the various approaches used in the studies, three qualitative levels of toxicity were considered: low, parasitoids are not significantly
affected; high, parasitoids suffer high mortality and/or population reduction; and moderated, effects are noticeable, but they are not very
strong, or are variable among generations, treatments, etc.

time, are potentially compatible with biological There are numerous studies on the susceptibility
control agents due to their low toxicity and high of leafminer parasitoids to different types
specificity. of insecticides (Table 1). Some species of
132 CIENCIA E INVESTIGACION AGRARIA

leafminer parasitoids have developed resistance, biological control in crops. These plant species
mainly to organophosphorates. For example, could be used for the implementation of open-
Diglyphus begini (Ashmead) (Hymenoptera: field rearing of parasitoids (Parkman et al.,
Eulophidae) is tolerant to oxamyl, methomyl, 1989), which consist of favoring the presence
permethrin, and fenvalerate (Rathman et al., of plants and harmless leafminers, in the same
1990). Insecticide application time and method environment as the crop, to increase populations
may affect the susceptibility of the parasitoids of natural enemies. Rearing parasitoids in the
(Kaspi and Parrella, 2005; Weintraub, 1999), open field has been successful for controlling
which varies between species (Mafi and some leafminers (van der Linden, 1992). For
Ohhayashi, 2006) and even between genders this, the knowledge of leafminer host ranges
(Rathman et al., 1992). and their parasitoids is critical (Parkman et al.,
1989; Chen et al., 2003b; Rizzo, 2003). In some
In studies with different leafminer species, cases, the study of trophic webs in different
crops treated with low doses or without environments has made possible the theoretical
insecticides had higher percentages of proposal of open-field rearing systems, taking
parasitoidism (Galantini Vignez and Redolfi de into account the possible interactions between
Huiza, 1992; van Driesche et al., 1998; Adachi, the species at three trophic levels (Valladares
2002; Chen et al., 2003a). Likewise, in organic and Salvo, 1999).
crops, greater parasitoid species richness along
with improved efficiency has been observed Policultures and planting additional plant
(Balzs, 1998). However, in other cases, there species with the main crop may also have a
was no difference on leafminer parasitoid positive effect on parasitoids. For example, it
densities between plots treated and not has been observed that at the beginning of the
treated with synthetic insecticides (Mafi and sweet potato crop cycle, growing kidney bean
Ohbayashi, 2004). plants in adjacent strips attracts L. huidobrensis
parasitoids, and advances and increases their
Parasitoids and cultural control presence in the sweet potato crop (Da Paixo
Pereira et al., 2002). Likewise, potato cultivated
It is possible to increase the action of leafminer along with wheat has less leafminer damage
enemies through habitat management (Price because wheat attracts parasitoids (Ebwongu et
and Harbaugh, 1981). Different studies mention al., 2001).
the importance of weed patches near crops as
possible reservoirs of parasitoids (Murphy and Adult parasitoid food provisioning, by means
La Salle, 1999). For this reason, it has been of sugar solutions or honey, is a conservation
suggested that the management of weeds and biological control practice that has been
other plants in or at the edge of an agroecosystem repeatedly used (Powell, 1986). However,
can improve the availability of pollen and nectar in some cases, the provision of food for the
for leafminers natural enemies (van Mele parasitoids of a primary pest can have a
and van Lenteren, 2002). In some cases, the negative impact on the control of secondary
presence of flowering plants in habitats nearby pests, to which leafminers generally belong to
produces an increase in leafminer parasitoidism (Mitsunaga et al., 2006).
(Chen et al., 2003b). However, in other cases,
the increase in plant diversity had no effect on Among biological control techniques that
leafminers or their parasitoids (Johnson and augment and conserve leafminers natural
Mau, 1986; Letourneau, 1995). enemies, physical devices have been designed to
allow parasitoids to escape, which are generally
Although some weeds may act as reservoirs smaller than their hosts, based on containers
of leafminer pests (Smith and Hardman, 1986; with mined leaves (Kehrli et al., 2005). This
Schuster et al., 1991), others give refuge to apparatus serve to augment or conserve local or
leafminer specialists, which do not harm crops. foreign parasitoid populations and could be a low
In the latter case, weeds provide alternative cost alternative to the release of conventionally
hosts for the parasitoids, thereby increasing the reared natural enemies. This method can be
VOL 34 N3 SEPTEMBER - DECEMBER 2007 133

used where chemical control is forbidden, like sticky surfaces, play a double role, monitoring
in the case of organic agriculture. By making leafminer populations (to learn the appropriate
adjustments in screen size, diverse parasitoid time to apply some type of control), and at the
and host systems can be managed in this way same time, decrease the number of leafminers
(Kehrli and Bacher, 2004). in a field (Larran, 2004). These traps are
used in integrated pest management programs
It is important to keep in mind that although for leafminer flies (Agromyzidae), where the
some practices recommended that leafminer number and surface area of traps for effective
control favor the increase of parasitoid control is known in some detail (Braun and
populations, others harm them. For example, Shepard, 1997). However, there is a possibility
flooding to drown pupae of certain leafminers, that yellow sticky traps decrease parasitoid
or sunlight exposition of pupae to provoke their populations (Gonalves, 2006). The combination
death also reduces populations of larvo-pupal of yellow traps with attractive substances for
parasitoids (Braun and Shepard, 1997). the leafminers, such as extracts of host plant
leaves, notably decreases the capture of other
Compost application to the crop may have insects and possibly also reduces the number of
an indirect effect on leafminers, increasing parasitoids trapped there (Harand et al., 2004).
their predators diversity and efficiency
(Brown and Tworkoski, 2004). However, Integrated pest and leafminer management
nitrogen fertilizers must be used with care
because they can stimulate pest development, The integration of various practices in integrated
augmenting not only the plants vigor, but also pest management programs has proven to be
the survival of leafminer larvae and pupae successful in the control of leafminers. The
(van Lenteren and Overholt, 1994). There replacement of synthetic chemical pesticides
might be fertilization thresholds above which by biopesticides (i.e. Bacillus thuringiensis) s
the numbers of leafminer pupa are augmented or the selective use of insecticides with low
and the parasitoidism diminishes, as shown in impact on the natural enemies, the decrease of
citrus leafminers (Ateyyat and Mustafa, 2001). disturbances imposed in the system (through
On the other hand, elevated levels of nitrogen less aggressive agricultural practices), and
fertilization in kidney bean crops decreased the the implementation of the different types of
development time and increased the fertility biological control all increase the chances of
of the parasitoid Chrysocharis oscidinis controlling leafminers (Murphy and La Salle,
(Hymenoptera: Eulophidae) on the leafminer 1999).
Liriomyza trifolii (Kaneshiro and Johnson,
1996). Other studies have evaluated the effect Laboratory experiments with cages demonstrate
of fertilization on parasitoidism rates, without that the release of Diglyphus isaea together
analyzing the mechanisms involved (Yarnes with the release of sterile male L. huidobrensis
and Boecklen, 2006). constitutes a more efficient method than the use
of each technique separately (Kaspi and Parrella,
One practice recommended for reducing 2006). Some parasitoids can develop in eggs laid
leafminer populations is the destruction of by females sterilized by gamma rays, even over
plant residues from the previous harvests that several generations (Harwalkar et al., 1987).
were attacked by pests, which can be burned
or buried (Larran, 2004), but this practice Diverse studies have undertaken the
also reduces parasitoid populations (Vincent et implementation of integrated pest management
al., 2004). However, pruning during summer programs for the control of leafminers,
and placing the cut branches under the trees including models and detailed costs-benefit
resulted in a decrease in the number of citrus analyses (Dudley et al., 1989; Shepard et al.,
leafminer larvae and pupae without affecting 1998; Gelernter and Trumble, 1999; Reitz et
parasitoidism (Ateyyat and Mustafa, 2001). al., 1999; Motta Miranda et al., 2005). They
agree that it is possible to markedly decrease
Sticky traps, consisting usually of yellow the amount of pesticides applied compared
134 CIENCIA E INVESTIGACION AGRARIA

to calendar applications. For example, the employed for leafminer pest control.
integrated pest management programs for L.
huidobrensis in Per include the use of resistant Resumen
or tolerant varieties, irrigation management,
elimination of harvest waste, sticky yellow Los minadores de hojas son insectos cuyas
traps, insecticides with low toxicity, and larvas viven y se alimentan dentro de las hojas,
biological control (Palacios et al., 1995). In consumiendo el mesfilo sin daar la epidermis
greenhouses, the application of adulticides (i.e. foliar. Varias especies son consideradas serias
pyrethroids) to reduce the initial populations plagas de cultivos intensivos, hortcolas y
of the miner pest, in combination with two ornamentales. Entre las fuentes de mortalidad
or three applications of selective insecticides, ms importantes para este gremio de fitfagos
such as azadirachtin, minimizes the possibility se citan a los enemigos naturales, de los que se
of resistance and ensures the control of all the destacan los parasitoides como el grupo ms
stages of the pest without obstructing the action efectivo y mejor representado. Este artculo
of natural enemies, extending the control range proporciona un resumen actualizado de la
(Immaraju, 1998). informacin disponible sobre parasitoides de
minadores de hojas en relacin al manejo de
Conclusion plagas. Por ser generalistas, los parasitoides de
minadores de hojas pueden incluir rpidamente
As a conclusion, is important to emphasize that en su rango alimenticio a especies introducidas,
there are abundant bibliographic records that muchas veces logrndose un control efectivo
detail the relationship between parasitoids and luego de unos pocos aos de establecida la
leafminers. They include descriptive biological plaga. Control biolgico clsico y aumentativo
or ecological aspects without direct relation son estrategias ampliamente usadas para regular
to the management of pest species, studies las poblaciones de minadores de hojas plaga.
which were not included here because they Numerosos estudios abordan la compatibilidad
were beyond the objective of this review. Also, del uso de parasitoides con control qumico y
there are numerous practical studies available cultural. Si bien la mayora de los insecticidas
that analyze the compatibility of parasitoid use convencionales poseen efectos adversos para
combined with different chemical pesticides, as los parasitoides, otros seran compatibles con el
explained above. control biolgico. Se conoce que la combinacin
de diversas estrategias de control en programas
The areas that are less developed are those de manejo integrado de plagas ha resultado
that explore the importance of the different efectivo contra minador de hojas plaga. Sin
sources of mortality in leafminer life tables embargo, los efectos de prcticas culturales
and the impact of agricultural practices on the que podran favorecer las poblaciones de
parasitoid fauna. In this regard, the effect of parasitoides han sido escasamente estudiados.
nearby weeds on the parasitoids is practically
unknown, and information referring to the Palabras clave: Control biolgico, control
interaction of pest parasitoids with other cultural, control qumico, minadores de hojas,
hosts in the agroecosystem is also scarce. parasitoides.
To have this type of information available,
especially incorporating information on the Acknowledgments
three trophic levels involved: plants (cultivation
and spontaneous vegetation), leafminers (pest We would like to express our gratitude to the
and alternative hosts), and parasitoids, would following institutions that have supported
make the implementation of ecologically the development of this research: CONICET,
sound management strategies possible. Open- SECYT, FONCYT. We also thank W. A. Quispe
field parasitoid rearing systems, management Avalos for reading the original manuscript
of plant diversity, and other environmental and M. S. Fenoglio (Entomological Research
manipulation methods, constitute, in this sense, Center, Universidad Nacional de Crdoba) for
alternatives that have been, up to now, scarcely the photographic work.
VOL 34 N3 SEPTEMBER - DECEMBER 2007 135

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